Fisheries, low oxygen and climate change: how much do we really know?

As a result of long-term climate change, regions of the ocean with low oxygen concentrations are predicted to occur more frequently and persist for longer periods of time in the future. When low levels of oxygen are present, this places additional pressure on marine organisms to meet their metabolic requirements, with implications for growth, feeding and reproduction. Extensive research has been carried out on the effects of acute hypoxia, but far less on long-term chronic effects of low oxygen zones, especially with regard to commercially important fishes and shellfishes. To provide further understanding on how commercial species could be affected, the results of relevant experiments must support population and ecosystem models. This is not easy because individual effects are wide-ranging; for example, studies to date have shown that low oxygen zones can affect predator-prey relationships as some species are able to tolerate low oxygen more than others. Some fishes may move away from areas until oxygen levels return to acceptable levels, while others take advantage of a reduced start response in prey fishes and remain in the area to feed. Sessile or less mobile species such as shellfishes are unable to move out of depleted oxygen zones. Some species can tolerate low oxygen levels for only short periods of time, while others are able to acclimatize. To advance the knowledge-base further, a number of promising technological and modelling-based developments and the role of physiological data within these, are proposed. These include advances in remote telemetry (tagging) and sensor technologies, trait-based analyses to provide insight into how whole assemblages might respond in the future, research into long-term adaptability of species, population and ecosystem modelling techniques and quantification of economic effects. In addition, more detailed oxygen monitoring and projections are required to better understand the likely temporal and local-scale changes in oxygen.

Recent advances in telemetry for estimating the energy metabolism of wild fishes.

Metabolic rate is a critical factor in animal biology and ecology, providing an objective measure that can be used in attributing a cost to different activities and to assessing what animals do against some optimal behaviour. Ideally, metabolic rate would be estimated directly by measuring heat output but, until recently, this has not been easily tractable with fishes so instead metabolic rate is usually estimated using indirect methods. In the laboratory, oxygen consumption rate is the indirect method most frequently used for estimating metabolic rate, but technical requirements preclude the measurement of either heat output or oxygen consumption rate in free-ranging fishes. There are other field methods for estimating metabolic rate that can be used with mammals and birds but, again, these cannot be used with fishes. Here, the use of electronic devices that record body acceleration in three dimensions (accelerometry) is considered. Accelerometry is a comparatively new telemetric method for assessing energy metabolism in animals. Correlations between dynamic body acceleration (DBA) and oxygen consumption rate demonstrate that this will be a useful proxy for estimating activity-specific energy expenditure from fishes in mesocosm or field studies over extended periods where other methods (e.g. oxygen consumption rate) are not feasible. DBA therefore has potential as a valuable tool for attributing cost to different activities. This could help in gaining a full picture of how fishes make energy-based trade-offs between different levels of activity when faced with conflicting or competing demands arising from increased and combined environmental stressors.

Conservation physiology for applied management of marine fish: an overview with perspectives on the role and value of telemetry.

Physiological studies focus on the responses of cells, tissues and individuals to stressors, usually in laboratory situations. Conservation and management, on the other hand, focus on populations. The field of conservation physiology addresses the question of how abiotic drivers of physiological responses at the level of the individual alter requirements for successful conservation and management of populations. To achieve this, impacts of physiological effects at the individual level need to be scaled to impacts on population dynamics, which requires consideration of ecology. Successfully realizing the potential of conservation physiology requires interdisciplinary studies incorporating physiology and ecology, and requires that a constructive dialogue develops between these traditionally disparate fields. To encourage this dialogue, we consider the increasingly explicit incorporation of physiology into ecological models applied to marine fish conservation and management. Conservation physiology is further challenged as the physiology of an individual revealed under laboratory conditions is unlikely to reflect realized responses to the complex variable stressors to which it is exposed in the wild. Telemetry technology offers the capability to record an animal's behaviour while simultaneously recording environmental variables to which it is exposed. We consider how the emerging insights from telemetry can strengthen the incorporation of physiology into ecology.

Welfare in wild-capture marine fisheries.

In contrast to terrestrial farming or aquaculture, little, if any, welfare regulation exists that constrains how fishes are handled or killed in wild-capture marine fisheries. Given that welfare in wild-capture fisheries is moving further up the public agenda, an unbiased, dispassionate account of what happens to fishes caught in wild-capture marine fisheries is needed so as to identify where the main animal welfare issues exist.

The diving behaviour of green turtles undertaking oceanic migration to and from Ascension Island: dive durations, dive profiles and depth distribution.

Satellite telemetry was used to record the submergence duration of green turtles (Chelonia mydas) as they migrated from Ascension Island to Brazil (N=12 individuals) while time/depth recorders (TDRs) were used to examine the depth distribution and dive profiles of individuals returning to Ascension Island to nest after experimental displacement (N=5 individuals). Satellite telemetry revealed that most submergences were short (<5 min) but that some submergences were longer (>20 min), particularly at night. TDRs revealed that much of the time was spent conducting short (2-4 min), shallow (approximately 0.9-1.5 m) dives, consistent with predictions for optimisation of near-surface travelling, while long (typically 20-30 min), deep (typically 10-20 m) dives had a distinctive profile found in other marine reptiles. These results suggest that green turtles crossing the Atlantic do not behave invariantly, but instead alternate between periods of travelling just beneath the surface and diving deeper. These deep dives may have evolved to reduce silhouetting against the surface, which would make turtles more susceptible to visual predators such as large sharks.

Effects of systemic hypoxia on the distribution of cardiac output in the rat.

1. Studies were made in unanaesthetized rats of cardiovascular responses induced during 3 min periods of systemic hypoxia (inspirate 8 or 6% O2). Arterial pressure and heart rate were recorded continuously; cardiac index and regional blood flows were measured in normoxia and at the 2nd min of hypoxia by injection of radiolabelled microspheres. Comparisons are made with changes recorded in Saffan-anaesthetized rats during 8% O2 using microspheres and in previous studies using electromagnetic transducers on renal, mesenteric and femoral arteries (Marshall & Metcalfe, 1988a). 2. In unanaesthetized rats, the initial 1-1.5 min of hypoxia evoked behavioural arousal associated with a short-lasting rise in arterial pressure and heart rate. This agrees with our previous proposal that hypoxia activates the brain stem defence areas by stimulating peripheral chemoreceptors. 3. In unanaesthetized rats, these changes were superimposed upon a gradual fall in arterial pressure and tachycardia, the responses being greater during 6 than 8% O2 (cf. Saffan-anaesthetized rats). Further, in all rats at the 2nd min of hypoxia, cardiac index and vascular conductance of most body tissues was increased. It is concluded that the fall in arterial pressure is due to peripheral vasodilatation. 4. In the unanaesthetized rats, the tendency for vascular conductance in kidney, intestine and gastrocnemius muscle to increase (more during 6 than 8% O2) allowed increases in blood flow in the last two regions. These changes accord with those recorded under Saffan anaesthesia. 5. In both unanaesthetized and anaesthetized rats, hypoxia induced pronounced increases in vascular conductance of diaphragm, adrenal gland, cerebral hemispheres, cerebellum and brain stem, the resultant increases in blood flow being larger in the unanaesthetized rats. 6. It is proposed that in unanaesthetized, as in anaesthetized, rats the regional dilator responses predominantly reflect the local dilator effects of tissue hypoxia. Possible dilator factors are considered.

Analysis of factors that contribute to cardiovascular changes induced in the cat by graded levels of systemic hypoxia.

1. In cats anaesthetized with Saffan, which does not block afferent activation of the brain stem defence areas, we have analysed the cardiovascular changes induced by 3 min periods of graded systemic hypoxia (fraction of O2 in inspirate, Fi,O2, 0.15, 0.12, 0.08, 0.06). 2. At light levels of Saffan anaesthesia, hypoxia (particularly Fi, O2 0.08 and 0.06) or selective stimulation of carotid chemoreceptors evoked the pattern of tachycardia, decrease in renal and mesenteric vascular conductance (RVC, MVC), but increase in femoral vascular conductance (FVC) which is characteristic of the alerting-defence response. This supports our view that activation of the defence areas is an integral part of the response to systemic hypoxia. 3. Hypoxia also induced an increase in frequency of augmented breaths which was graded with the level of hypoxia: 0.6 min-1 at Fi, O2 0.21 to 1.1 min-1 at Fi, O2 0.06; in some cats each of these was accompanied by a transient fall in arterial pressure (ABP) and increase in FVC. It is proposed that these responses were all part of a reflex elicited by lung irritant receptors and facilitated by peripheral chemoreceptors. However, their low rate of occurrence and the liability of the vasodilatation suggests they do not make major contributions to the overall response. 4. The above short-lasting responses were superimposed upon gradual changes whose magnitudes were graded with the level of hypoxia: hyperventilation, slight tachycardia, but bradycardia at Fi, O2 0.6, small increases in ABP, FVC and MVC allowing femoral and mesenteric blood flow to increase, but decreases in RVC which maintained renal blood flow constant. 5. Vagotomy had no significant effect on these changes. Further, hyperinflation of the lungs with pressures of 10 mmHg evoked the Breuer-Hering reflex but had no noticeable cardiovascular effect. It is proposed that, in the cat, reflex tachycardia and vasodilatation elicited by lung stretch receptors play no significant part in the response to hypoxia. 6. By contrast, after pneumothorax, with ventilation and thereby arterial PCO2 (Pa, CO2) maintained constant, graded hypoxia produced graded bradycardia, decrease in MVC and RVC and no change in FVC. Taken together, these results suggest that in the spontaneously breathing cat, the response to hypoxia is dominated by the effects of hypocapnia secondary to hyperventilation, which by inhibiting peripheral and central chemoreceptor activity effectively counteracts the primary bradycardia and peripheral vasoconstriction elicited by hypoxic stimulation of peripheral chemoreceptors. 7. These proposals are compared with those drawn for other species.

Influences on the cardiovascular response to graded levels of systemic hypoxia of the accompanying hypocapnia in the rat.

1. In spontaneously breathing, anaesthetized rats, a study was made of the effects upon the graded cardiovascular responses to systemic hypoxia (inspiratory fractional O2 concentration, Fi, O2: 0.15, 0.12, 0.08, 0.06) of maintaining arterial CO2 pressure (Pa,CO2) at the air-breathing level by adding CO2 to the inspirate (eucapnic hypoxia), rather than allowing Pa,CO2 to fall (hypocapnia hypoxia). 2. At each Fi,O2, maintenance of eucapnia significantly reduced the increase in respiratory frequency, but significantly accentuated the increase in tidal and minute volume: as a result the fall in Pa,O2 at each Fi,O2 was significantly reduced. 3. Concomitantly, maintenance of eucapnia reduced the increase in heart rate (HR) and fall in arterial pressure (ABP), the effects being significant at Fi,O2 0.08 and/or 0.06. There was also a tendency for the increases in renal and femoral vascular conductances (RVC, FVC) to be reduced; at Fi,O2 0.06 mean increases from control were 2 +/- 10 vs. 16 +/- 7% (eucapnia vs. hypocapnia) for RVC, and 62 +/- 11 vs. 106 +/- 27% for FVC. 4. As maintenance of eucapnia reduced the fall in Pa,O2 at each Fi,O2, the above results were also considered as a function of Pa,O2. Then, maintenance of eucapnia had similar significant effects on the changes in respiration and HR as described above and reduced the mean increase in RVC (16 +/- 11 vs. 23 +/- 10%, at Pa,O2 31 mmHg, which was attained at Fi,O2 0.06 with eucapnia and 0.08 with hypocapnia). However, maintenance of eucapnia had no effect on the falls in ABP and accentuated the mean increase in FVC (74.9 +/- 13 vs. 57 +/- 10% at Pa,O2 31 mmHg). 5. These findings indicate that, in the rat, the hypocapnia that accompanies the hyperventilatory response to systemic hypoxia facilitates the tachycardia and may accentuate the renal vasodilation, but attenuate the hypoxia-induced vasodilatation in skeletal muscle. Possible mechanisms are discussed.

Analysis of the cardiovascular changes induced in the rat by graded levels of systemic hypoxia.

1. In rats anaesthetized with Saffan, we have further analysed the respiratory, cardiac and regional vascular responses induced by 3 min periods of graded hypoxia (breathing 15, 12, 8 or 6% O2 in N2). 2. Frequently, hypoxia evoked an episode, lasting 1-1.5 min, of tachycardia, renal and mesenteric vasoconstriction and skeletal muscle vasodilatation. The tachycardia and muscle vasodilatation persisted after vagotomy indicating they were not initiated by pulmonary stretch receptors secondary to hyperventilation. We propose that such episodes represented the cardiovascular components of the alerting-defence response initiated by activation of the brain stem defence areas by peripheral chemoreceptors. 3. Each of these episodes was superimposed upon gradual hyperventilation, tachycardia, fall in arterial pressure and vasodilatation in renal, mesenteric and muscle circulation the magnitudes of which at 2 min were generally graded with the level of hypoxia. In the 3rd minute, respiration and heart rate tended to wane below control levels. 4. Vagotomy had little effect on the heart rate changes and only slightly reduced the peripheral vasodilatation allowing the conclusion that the gradual tachycardia and peripheral vasodilatation was not a reflex initiated by pulmonary stretch receptors. 5. Guanethidine given after vagotomy abolished the tachycardia indicating it was sympathetically mediated; possible initiating factors are discussed. But the secondary bradycardia persisted indicating it reflected the direct effect of hypoxia on cardiac pacemaker tissue. 6. The peripheral vasodilatation persisted after guanethidine or phentolamine indicating it was mainly attributable to the local vasodilator effects of tissue hypoxia. 7. It is proposed that the components of the alerting response are an integral part of the response to systemic hypoxia. Further, that in the rat this response is superimposed upon, but may be overcome by the direct effects of hypoxia on peripheral vasculature, heart and central nervous system.

Cardiovascular changes associated with augmented breaths in normoxia and hypoxia in the rat.

1. In the present study, anaesthetized rats showed respiratory gasps (augmented breaths) at regular intervals during air breathing and at increased frequency during hypoxia (breathing 15, 12, 8 or 6% O2 in N2). Each augmented breath was accompanied by transient vasodilatation in hindlimb skeletal muscle and sometimes bradycardia. In hypoxia these changes were superimposed upon more gradual muscle vasodilatation and tachycardia. 2. Both the augmented breaths and the transient muscle vasodilatations disappeared immediately after bilateral vagotomy but both sometimes reappeared 1-2 h later, particularly in hypoxia. 3. The transient vasodilatation in skeletal muscle sometimes preceded the augmented breath, indicating that the vasodilatation was not a reflex initiated by pulmonary stretch receptors secondary to the augmented breath. Moreover, hyperinflation of the lungs to 5-10 mmHg evoked the Breuer-Hering respiratory reflex but had no effect upon the cardiovascular variables. 4. Addition of SO2 (300-400 p.pm.) to the inspirate, which others have shown preferentially blocks pulmonary stretch receptors, abolished the Breuer-Hering reflex, but had no significant effect on baseline levels of muscle vascular conductance or heart rate during normoxia, nor on the gradual increases in these variables during hypoxia (8% O2). Moreover, augmented breaths still occurred during air breathing and during hypoxia, each being associated with transient muscle vasodilatation. 5. These results indicate that pulmonary stretch receptors have little reflex effect upon the cardiovascular system of the rat either in normoxia or hypoxia. Rather, we suggest that transient muscle vasodilatation and possibly bradycardia, as well as an augmented breath, are all part of a primary reflex, initiated by pulmonary irritant receptors, and facilitated by peripheral chemoreceptor stimulation, repetition of which is an integral part of the response to hypoxia.

Plasma catecholamines in the lesser spotted dogfish and rainbow trout at rest and during different levels of exercise.

The hypothesis that there is an increase in plasma catecholamines during exercise in fish and that they play an important role in the cardiovascular adjustments during exercise was investigated in the lesser spotted dogfish and rainbow trout. In resting fish plasma catecholamines were at a concentration of 10(-9)-10(-8) mol l-1. During spontaneous swimming in the dogfish, adrenaline increased by 3.3 times to 1.9 X 10(-8) mol l-1 and noradrenaline increased by 2.3 times to 3.2 X 10(-8) mol l-1. In rainbow trout swimming at a steady 1 body length s-1 (Ls-1) in a water channel, the levels of both amines decreased to approximately 25% of the resting values. When swimming to apparent exhaustion at approximately 2 Ls-1, adrenaline was 10 times the resting value at 1.4 X 10(-8) mol l-1, whereas noradrenaline was 2.2 times the resting value at 2.3 X 10(-8) mol l-1. Only after repeated burst swimming for 2-3 min did the levels of plasma catecholamines increase substantially above the resting values. In the dogfish, both amines were at 10(-7) mol l-1, whereas in the rainbow trout, noradrenaline was at 8.5 X 10(-8) mol l-1 and adrenaline was at 2 X 10(-7) mol l-1. These levels were compared with the concentrations of catecholamines used by other workers to elicit changes in the branchial vasculature, gas exchange at the gills or gas transport to the tissues. In lesser spotted dogfish, the levels of adrenaline and noradrenaline present in the plasma during spontaneous swimming have 80% and 50% of maximum effect on gill blood vessels, respectively, whereas in rainbow trout the levels present when swimming to apparent exhaustion have approximately 20% of maximum effect on the branchial vasculature. The levels present in the trout after repeated burst swimming have 40% of maximum effect on blood vessels in the gills. The difference between the dogfish and the trout may be related to the lack of innervation of the gill blood vessels in the former. Enhancement of gas exchange across the gills of rainbow trout can be demonstrated by using adrenaline at the concentration found after repeated burst swimming. It is possible, however, that the concentration of adrenaline found in the plasma of trout after swimming to apparent exhaustion may cause an increase in the concentration of oxygen in arterial blood, thus enhancing oxygen delivery to the tissues.(ABSTRACT TRUNCATED AT 400 WORDS)

Changes in activity and ventilation in response to hypoxia in unrestrained, unoperated dogfish (Scyliorhinus canicula L.).

daily activity cycles, together with changes in activity and ventilation frequency in response to hypoxia (PO2 about 8 kPa), have been measured in unrestrained, unoperated dogfish. Continuous recording of activity over 48 h reveals that dogfish are essentially nocturnal, being three to four times more active at night than during the day. In relatively inactive, diurnal dogfish, rapid reduction of environmental PO2 does not cause any significant increase in swimming activity, whereas prolonged hypoxia actually appears to suppress activity. In more active, nocturnal dogfish, rapid reduction of environmental PO2 causes an immediate reduction in activity which remains suppressed throughout the hypoxic period. It is concluded therefore that increases in circulating catecholamines in response to hypoxia are the result of hypoxia alone, rather than of any increase in locomotory activity. In resting diurnal dogfish, ventilation frequency is lower than has previously been reported for this species and, contrary to previous reports, increases markedly by 49% in response to hypoxia. It appears that in previous studies on confined dogfish, respiratory frequency, and probably ventilation volume, may have been elevated to near maximum levels even in 'resting' normoxic fish. This may have profound effects on so-called resting values for oxygen transfer in this species.

Differences between directly measured and calculated values for cardiac output in the dogfish: a criticism of the Fick method.

Cardiac output has been measured directly, and calculated by the Fick method, during normoxia and hypoxia in six artificially perfused dogfish (Scyliorhinus canicula) in an attempt to estimate the accuracy of this method in fish. The construction and operation of a simple extra-corporeal cardiac bypass pump is described. This pump closely mimics the flow pulse profiles of the fish's own heart and allows complete control of both cardiac stroke volume and systolic and diastolic periods. During normoxia (PO2 = 21 kPa) there was no significant difference between directly measured and calculated values for cardiac output. However, some shunting of blood past the respiratory surface of the gills may have been obscured by cutaneous oxygen uptake. In response to hypoxia (PO2 = 8.6 kPa) there is either a decrease in the amount of blood being shunted past the respiratory surface of the gills and/or an increase in cutaneous oxygen uptake such that the Fick calculated value for cardiac output is on average 38% greater than the measured value. It is proposed that the increase in the levels of circulating catecholamines that is reported to occur in response to hypoxia in this species may play an important role in the observed response to hypoxia. The results are discussed in terms of their implications for the calculation of cardiac output by the Fick principle in fish.